Download The Emergence of Disease Ecology

特集：野生動物医学の新展開 “Disease Ecology” とはどのような学問分野か
第 21 回日本野生動物医学会大会　日本野生動物医学会 IWMC2015 連携公開シンポジウム
2015 年 7 月 31 日（金）
The Emergence of Disease Ecology
Shannon L. LADEAU ＊ and Barbara A. HAN
Cary Institute of Ecosystem Studies, 2801 Sharon Turnpike, Millbrook, NY, U.S.A., 12545
［Received 15 February 2016; accepted 8 April 2016］
ABSTRACT
The number of newly recognized diseases affecting humans, domestic animals and wildlife has increased in recent
decades and many of these diseases 'emerge' when environmental conditions change to alter contact rates between
species. While traditional disease biology or epidemiological studies strive to understand the patterns of outbreak
in a single species of interest, it is increasingly evident that management strategies demand more comprehensive
understanding of the ecological interactions across wildlife, human, domestic animal and potential vector populations.
This paper will introduce the ecological principles underlying pathogen dynamics in ecological systems and highlight
current research frontiers in Disease Ecology. Pathogens and parasites are often considered as a disturbance rather than
an inherent part of ecological systems, yet the fundamental principles of disease ecology derive from classical theory in
population and community ecology.
Key words: community, dynamical models, ecosystem, pathogen, zoonotic
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There are often complex but predictable ecological dynamics
understanding to significantly advance management and
that define when pathogens lead to disease, such as changes
forecasting capacity in many disease systems.
in interactions between hosts, contact rates with the pathogen,
FUNDAMENTAL PRINCIPLES
and host susceptibility. However, pathogens exist in natural
systems well before humans detect them. For example, Vibrio
The fundamental principles of disease ecology derive from
cholerae occurs naturally in copepod hosts across many
classical theory in population and community ecology. Ecology
aquatic environments [1]; yet environmental conditions that
may be summarized as the study of mechanisms controlling
influence population growth and community interactions in
population growth and species coexistence. Likewise, disease
these copepod communities can change the system to result in
ecology is the study of mechanisms controlling the growth
human cholera epidemics [2, 3]. The focus on disease ecology
of infected host populations, which relies on understanding
as an explicit discipline has been relatively recent, with a six-
how individuals, populations and species interact to support
fold increase in peer-reviewed articles in the past twenty-
pathogen transmission. In Fig. 1, susceptible hosts (S)
five years. This growing field embraces theory developed in
transition to the infected state (I) with transmission probability
population and community ecology to guide both empirical
(β). This is the SIR model framework used as the conceptual
and theoretical research aims centered on understanding
backbone for much of the mechanistic modeling of infectious
pathogen transmission and host health impacts. This paper
disease in humans [4]. Generating forecasts or inference in
summarizes how disease ecology derives from fundamental
real-world systems may require integration of demography,
ecological principles and highlights the potential for ecological
as well as environmental variability and stochasticity into this
conceptual model [5-10]. The oft-cited threshold parameter
* Corresponding author：
Shannon LaDeau（E-mail : [email protected]）
(R0), describing the likely number of newly infected individuals
generated by the introduction of a single infected host into a
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Shannon L. LADEAU and Barbara A. HAN
S
β
I
γ
filters that influence the population growth of hosts, vectors,
and pathogens. One example of environmental complexity
R
supporting pathogen dynamics is seen in the tick-borne Lyme
Fig. 1 Dynamical systems models (e.g., SIR) simplify
epidemiological theory into a series of transition equations. For
the past century, this structure has been the core of infectious
disease models and management strategies [4, 29, 30]. Model
estimates for transition from susceptible (S) to infected (I)
states are described by a transmission term (β); contact
rates are often assumed to be constant and random across
individuals. Transmission is also a function of the duration of
Disease system of the northeastern United States, where
pathogen abundance can be linked to seasonal variability in
food resources supporting reservoir host populations (Fig.
2). Fig. 2 doesn’t include the meso-predator species (e.g.,
Vulpes vulpes , red fox) or alternative hosts such as opossums
(Didelphis virginiana ) that help regulate mouse populations
and tick survival [15-17]. There are a complex suite of
mechanisms and interactions behind spatio-temporal patterns
infectiousness, as quantified by the recovery rate (γ).
pool of susceptibles, is derived from this conceptual model [11,
12].
SOME DEFINITIONS
Here, we refer to a pathogen as any causative agent of
disease that may be transmitted from one host to another.
If the pathogen may be transmitted from a non-human to a
human host then it is considered zoonotic. Vector organisms,
often blood-feeding arthropods, move a pathogen between
hosts. Host species are those organisms that are susceptible
to becoming infected with a pathogen. Hosts may either
become infected but remain asymptomatic, or they may
succumb to disease. In a multi-host system, a separate host
species that maintains a pathogen long-term without high
mortality is termed a reservoir host. An infected host may
become infectious and able to transmit the pathogen to
F i g . 2 T h e c a u s a t i ve a g e n t o f Lym e d i s e a s e i n t h e
another individual directly or through a vector species. If a
northeastern United States, Borrellia burgdorferi , is transmitted
host becomes infected but does not transmit a pathogen, it is
from an infected, often asymptomatic, reservoir species to
considered a dead-end host.
blacklegged ticks, Ixodes scapularis . The predominant reservoir
Pathogen transmission involves the interaction of at least
species is the white-footed mouse (Peromyscus leucopus ),
two organisms, the host and the pathogen itself. A zoonotic
whose abundance is a function of food availability each
pathogen may be transmitted to a human but predominantly
season. Mice eat acorns and during a mast year when oak
persists in another species. West Nile virus, for example
trees produce a superabundance of acorns, mouse populations
persists in avian reservoirs but can spill-over into humans
grow. High mouse abundance allows more ticks to survive to
when conditions permit, such as in urban habitat following
pass Borrellia on to larger animals, including deer and humans.
permissive weather [13, 14]. Traditional epidemiological
Additional complexity is evident when considering that high
studies predominantly examine the patterns of pathogen
mouse populations may also be supported by gypsy moth
infection in one host species of interest (often the human host).
outbreaks [31, 32], which could change oak tree populations
However, human infection is often the end result of a series of
and acorn availability. Graphic provided by Cary Institute of
interactions (i.e., competition, predation) and environmental
Ecosystem Studies.
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Disease Ecology
in disease incidence. Ecology provides a natural framework for
Inferring an unobserved transmission mechanism from
identifying and quantifying these dynamics.
imperfect observations of infection status requires innovations
in causal inference [18], and the development of modeling
RESEARCH FRONTIERS
frameworks that can handle latent process estimation [19].
Developing enough mechanistic understanding to identify
Integrating field data with transmission models to estimate
strategies for management or epidemic forecasting is a critical
critical infection, transmission and recovery rates in complex,
research goal. We identify three current research objectives for
multi-host or vectored systems is a critical goal for disease
the field of Disease Ecology - each of which acknowledges the
ecologists and public/wildlife health managers [20].
very real need for inference to develop predictions and guide
A second major focus for the field of Disease Ecology is
management. the development of theoretical models that are generalizable
Disease transmission among non-human animals is not
across disease systems. This theoretical guidance is critical for
easily studied in natural environments and the historical time
identifying important research directions and for extending
series that have supported many advances in human infectious
inference beyond the specific system, time and place of study.
disease research do not exist for wildlife populations. Thus,
Perhaps the most important theoretical discussion specific to
in many cases of wildlife or zoonotic disease we are missing
disease ecology is about the potential for species diversity to
observations of infection status as well as observations of
regulate pathogen abundance. The dilution effect hypothesis
transmission events. This is a challenge for understanding
proposes that pathogen abundance can be limited in more
wildlife disease systems and for predicting when or discovering
diverse host communities, especially when host susceptibility
how a zoonotic pathogen spills over into human populations.
is variable across multiple species [21]. A recent meta-analysis
Community X
e Encounter reduction
a Transmission reduction
b Susceptible host regulation
c Recovery augmentation
d Infected host mortality
Fig. 3　Conceptual model depicting mechanisms by which diversity could reduce disease risk in a specialist host–pathogen
system. The original Community X contains a single species with infected (filled circles) and uninfected, susceptible (open
circles) individuals. The filled grey circle in Community X denotes recent transmission event in the single-species community.
Individuals contact radius or home ranges are shown as dashed lines. The addition of a second species (black squares) could
(a) reduce the probability of transmission (via reduced pathogen load) per encounter between susceptible and infected hosts
(transmission reduction ); (b) reduce the number of susceptible hosts (susceptible host regulation ); (c) increase the rate of
recovery of infected individuals (recovery augmentation ); (d) increase the mortality rate of infected individuals (infected host
mortality ); or (e) reduce space used (contact radius) by the host species, reducing encounters between susceptible and infected
individuals (encounter reduction ). Redrawn from Fig. 1 in [21].
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Shannon L. LADEAU and Barbara A. HAN
used results from studies on 47 parasites that infect wildlife
NH, Mahmud A, Sack RB, Nair GB, Chakraborty J, Sack DA,
exclusively and 14 zoonotic pathogens to demonstrate a
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to understand when biodiversity conservation is unlikely to
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increasingly abundant data to identify the relevant reservoir
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a global health imperative. For example, machine learning
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species transmission and zoonotic spillover to humans.
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expertise with domain expertise in disease biology that zooms
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variation in infectious disease patterns across species.
Utility of R0 as a predictor of disease invasion in structured
ACKNOWLEDGEMENT
populations. J R Soc Interface 4: 315-324.
Shannon LaDeau is grateful to the Japanese Society of Zoo
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and Wildlife Medicine for the opportunity to present and
pathogens of wildlife. Philos T Roy Soc B 356: 1001-1012.
13. LaDeau SL, Calder CA, Doran PJ, Marra PP. 2011. West Nile
discuss research at their Annual Meeting in July 2015.
virus impacts in American crow populations are associated
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mathematical theory of epidemics. Part III. further studies of
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diversity on disease risk. Ecol Lett 9: 485-498.
the problem of endemicity. P Roy Soc Lond A Mat 141: 94122.
22. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J,
McMahon TA, Ortega CN, Sauer EL, Sehgal T, Young S, Rohr
JR. 2015. Biodiversity inhibits parasites: Broad evidence for
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Shannon L. LADEAU and Barbara A. HAN
Disases Ecology（疾病生態学）の出現
Shannon L. LADEAU ＊ and Barbara A. HAN
Cary Institute of Ecosystem Studies, 2801 Sharon Turnpike, Millbrook, NY, U.S.A., 12545
［2016 年 2 月 15 日受領，2016 年 4 月 8 日採択］
要　約
ここ数十年間，ヒトや家畜，野生動物において新たに確認される疾病の数は増加している。これらの疾病の多くは，環境条件が
変化した結果，生物種間の接触頻度が変わることで “emerge 現れる” のである。従来の疾病生物学あるいは疫学研究は，対象と
なる 1 つの生物種におけるアウトブレイクパターンを理解しようとするものである。しかしながら，疾病管理対策には，野生動
物，ヒト，家畜，そして潜在的な媒介動物集団にまたがる生態学的相互作用について，より包括的な理解が必要であることが，
ますます明らかになってきている。本論文では，生態系における病原体動態の根底にある生態学的原則について紹介し，“disease
ecology” 分野の最前線の研究について取り上げる。病原体や寄生虫は，生態系に固有のものであるというよりはむしろ生態系を
乱すものと考えられがちであるが，“disease ecology” の基本原理は，個体群および群集生態学の古典論に由来するものである。
キーワード：エコシステム，群集，人獣共通感染症，動態モデル，病原体
－日本野生動物医学会誌 21
（3）
：53-58，2016
* 責任著者：
Shannon LaDeau（E-mail : [email protected]）
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